Download Homogenization, Differentiation, and the Widespread Alteration of

American Fisheries Society Symposium 73:311–326, 2010
© 2010 by the American Fisheries Society
Homogenization, Differentiation, and the Widespread
Alteration of Fish Faunas
Frank J. Rahel*
Department of Zoology and Physiology and the Program in Ecology
Department 3166, 1000 East University Avenue
University of Wyoming, Laramie, Wyoming 82071, USA
Abstract.—Widespread introduction of common species coupled with extirpation of endemic species can cause fish assemblages to lose much of their regional
uniqueness. This process of biotic homogenization contrasts with biotic differentiation, whereby initially similar fish faunas diverge due to introductions of different
species. The relative importance of homogenization and differentiation in altering
fish faunas has been examined across the world. Synthesis of these studies indicates that homogenization of fish faunas has been widespread and that introductions, especially of sport fishes, have played a bigger role in altering fish faunas than
extirpations. In the United States, pairs of states now average 15.4 more species
in common than before European settlement. Additionally, the 89 pairs of states
that formerly had no fish species in common now share an average of 25.2 species. While homogenization is prevalent at large spatial scales, differentiation of fish
faunas is evident at intermediate spatial scales such as among watersheds within an
ecoregion. This differentiation is largely the result of the idiosyncratic nature of fish
introductions among individual lakes and streams. In general, translocated species
(i.e., species that are native somewhere in the region but that have been moved to
new locations) cause homogenization, whereas exotic species (species not native to
the region) cause differentiation. Habitat and flow homogenization are major drivers of biotic homogenization because altered habitats create conditions that favor a
few generalist species at the expense of more-specialized endemic species.
Introduction
Homogenization and differentiation are two
processes by which humans have altered spatial patterns in the similarity of biotic assemblages. Homogenization refers to an increase
in the similarity of biotas and differentiation
to a decrease in the similarity of biotas over
time. Natural processes such as glaciation,
stream capture, the formation of land bridges,
* Corresponding author: [email protected]
and speciation can alter spatial patterns in biotic similarity, but these operate over relatively
long periods. By contrast, humans have greatly
accelerated changes in biotic similarity by increasing colonization and extinction rates, by
simplifying and degrading habitats, and by enabling species to bypass historic biogeographic
barriers (Olden 2006; Rahel 2007). Whether
homogenization or differentiation occurs depends on the relative frequency of introductions versus extirpations, the spatial scale of
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the analysis, and the types of species being
introduced. Biologists are concerned about
homogenization because it often signals the
loss of unique species and their replacement
by cosmopolitan generalists (McKinney and
Lockwood 1999; Scott 2006). Although local
biodiversity may be enhanced through species
introductions, such artificial diversity often involves taxa that are already widespread, tolerant of degraded habitats, and considered to be
a nuisance by humans (Angermeier 1994; Pimentel et al. 2000; Scott and Helfman 2001).
Biotic differentiation is of concern because it is
usually the result of disparate localized introductions of species that often spread beyond
the original introduction site (Rahel 2004;
Clavero and García-Berthou 2006). Loss of
native species and gain of nonnative species
moves communities away from their natural
state and thus away from the conditions that
are most desired from a conservation perspective (Angermeier 2000).
Much of the literature on biotic homogenization has focused on quantifying how the
species composition of disjunct regions has
become more similar. However, the process of
homogenization extends across multiple levels
of biological organization, including genetic,
taxonomic, and functional homogenization
(Olden et al. 2004). Habitat homogenization
has resulted in similar aquatic habitats across
North America, such as eutrophic urban
ponds, warmwater reservoirs, cold tailwaters
below dams, and streams with relatively constant flow regimes (Moyle and Mount 2007).
In these human-created habitats, endemic species typically are replaced by cosmopolitan
species with the result that entire ecosystems
resembling each other now occur in disparate
parts of the country. Thus, common carp Cyprinus carpio, bullheads Ameiurus spp., and
aquarium fishes such as goldfish Carassius auratus inhabit many city ponds (Copp 2005;
Chizinski et al. 2006). Popular sport fish such
as largemouth bass Micropterus salmoides and
walleye Sander vitreus are the dominant species in reservoirs across North America (Rahel
2000; Taylor et al. 2001; Marchetti et al. 2006).
Even southern regions in the United States can
boast of trout fisheries where reservoirs release
cold hypolimnetic water throughout the summer (Quinn and Kwak 2003). At the genetic
level, homogenization of gene pools is of concern for taxa subject to artificial propagation
and widespread stocking, such as many species
of salmonids (Williamson and May 2005).
In this chapter, I discuss empirical patterns
in the homogenization and differentiation of
fish faunas and consider the mechanisms that
produce these patterns. Next, I discuss why we
should be concerned about human-mediated
changes in biotic similarity. In particular, what
are the ecological and evolutionary consequences of altering spatial patterns in biodiversity? Finally, I explore options for slowing the
rate of biotic homogenization and differentiation and consider if these processes can be reversed. Much of the literature on homogenization is focused on fish, but the principles apply
to other aquatic faunas and, in many cases, to
terrestrial taxa as well.
Quantifying Homogenization and
Differentiation
A variety of methods have been used to examine changes in spatial patterns in similarity
among fish assemblages (Table 1). Because
only presence–absence data are usually available, most studies have used a binary coefficient to quantify changes in similarity among
sites. The most commonly used coefficient is
Jaccard’s index, which is calculated as S = [a/
(a + b + c)] × 100, where S is the similarity between two sites and a = the number of species
found in both sites, b = the number of species
homogenization and differentiation of fish faunas
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Table 1. Studies examining homogenization and differentiation of fish faunas.
Author
Study area
Similarity metric
Findings
1. Radomski and 72 lakes in Minnesota
Jaccard Index
Homogenization due to
Goeman 1995 cosmopolitan introductions
2. Rahel 2000
48 coterminous states in the Jaccard index
Homogenization due to
United States cosmopolitan introductions
3. Duncan and
7 geographic provinces in
Spatial turnover
Homogenization predicted to
Lockwood 2001 Tennessee index (Ts) occur
4a. Marchetti et al.
6 zoogeographic provinces
Jaccard index
Homogenization due to
2001 in California cosmopolitan introductions
4b. Marchetti et al.
watersheds within provinces Jaccard index
Differentiation due to
2001 in California idiosyncratic introductions
5. MacRae and
14 lakes in Ontario
Ordination by Homogenization due to
Jackson 2001 correspondence predator introductions
analysis
6. Gido et al. 2002
14 sites in Big Blue River
Jaccard index
Homogenization mainly due
basin, Kansas to species introductions
7. Walters et al.
30 streams in Etowah River Ratio of endemic to
Homogenization due to loss
2003 basin, Georgia cosmopolitan of rheophilous species
species
8a. Taylor 2004
13 Canadian provinces and Jaccard index
Homogenization due to
territories cosmopolitan introductions
8b. Taylor 2004
8 ecoregions within British
Jaccard index
Differentiation due to
Columbia idiosyncratic introductions
9. Clavero and
10 Iberian basins in
Jaccard index
Homogenization due to
García-Berthou Europe cosmopolitan introductions
2006 10. Habit et al. 2006
Longitudinal patterns along Shannon-Wiener Homogenization due to
Biobio River, Chile
diversity index (H’) introductions and
extirpations
11. Marchetti et al.
Watersheds in 4 California
Ordination by Differentiation due to
2006 zoogeographic provinces multidimentional idiosyncratic introductions
scaling
12. Eberle 2007
2 river basins in Kansas
Unnamed similarity Homogenization due to
coefficient introductions and
extirpations
13a. Hoagstrom et al. 2 zoogeographic provinces Jaccard & Sorenson
Homogenization due to
2007 in South Dakota introductions and
extirpations
13b. Hoagstrom et al. 16 river drainages in South
Jaccard & Sorenson
Homogenization due to
2007 Dakota introductions and
extirpations
14. Leprieur et al. 25 river basins across
Jaccard index
Homogenization due to
2008 Europe translocated species
15a. Olden et al.
12 primary river basins
Sorensen index
Homogenization due to
2008 across Australia cosmopolitan introductions
15b. Olden et al.
53 secondary river basins in Sorensen index
Differentiation due to
2008 northeast Australia idiosyncratic introductions
16. Gido et al. Streams versus reservoirs in Bray-Curtis coefficient, Faunal homogenization
2008 Midwestern USA Jaccard index, followed conversion of
ordination by stream habitat to reservoir
nonmetric habitat
multidimensional
scaling
17. Casatti et al.
Agricultural versus natural
Bray-Curtis coefficient Habitat homogenization led 2009 to stream reaches in faunal homogenization by
Brazil nonnative species
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found only in the first site, and c = the number
of species found only in the second site. Values
of Jaccard’s index range from 0% (no species in
common) to 100% (complete overlap in species composition). Typically, the average similarity among a set of sites based on historical
fish species composition is subtracted from the
average similarity based on present-day fish
species composition. Positive values indicate
increased similarity (i.e., homogenization),
whereas negative values indicate decreased
similarity (i.e., differentiation).
Ordinations also can be used to visualize
changes in similarity patterns. Ordination axes
represent gradients of fish assemblage change,
and thus fish assemblages that are similar in
composition will cluster together in the ordination plot, whereas fish assemblages that differ in their composition will be dispersed. For
example, the close positioning of historical fish
assemblages in 10 Southern California watersheds indicates that they had similar fish faunas (Figure 1). By contrast, the dispersion of
the watersheds today indicates reduced similarity among their fish faunas. Marchetti et al.
(2006) attributed this differentiation to the id-
Axis 2
1.0
0.0
-1.0
-1.0
0.0
1.0
2.0
Axis 1
Figure 1. Ordination using nonmetric multidimensional scaling for 10 watersheds in Southern
California based on fish species composition at
two time periods. Historical (pre-1850) watershed
species composition is given as closed circles and
present-day species composition is given as open
circles (from Marchetti et al. 2006). The stress
value for the plot is 0.07.
iosyncratic nature of fish species introductions
among the watersheds. Gido et al. (2009) used
ordination to compare the similarity of fish assemblages in reservoirs versus streams in the
Great Plains, USA. In the ordination plot, reservoirs were clustered and stream sites were
dispersed, indicating that reservoirs contained
more homogenous fish faunas than streams
within the same drainages. Gido et al. attributed this to the fact that reservoirs were dominated by a small group of species introduced for
sportfishing, whereas stream sites retained the
diverse fish faunas that reflected the historical
biogeography of the region.
Walters et al. (2003) used the ratio of endemic to cosmopolitan fish species to examine
homogenization of fish faunas throughout the
Etowah River basin in Georgia, USA. The ratio
declined with increases in sedimentation and
eutrophication because unique benthic fishes
were replaced by widespread fishes tolerant of
degraded water quality. The loss of endemics
resulted in the homogenization of fish assemblages throughout the basin. An advantage of
the ratio used by Walters et al. is that it did not
require historical data on species composition.
However, there may be some subjectivity in
defining “endemic” versus “cosmopolitan” species. Using the ratio of endemic to cosmopolitan species based on abundance information
would be a way to detect the early stages of homogenization related to habitat degradation.
Sensitive species would be expected to decline
and generalist species would be expected to
increase well before extirpations of natives or
introductions of nonnatives becomes widespread.
Whatever method is used to quantify homogenization, it is important to recognize that
species changes do not necessarily cause predictable changes in assemblage similarity. Introductions and extirpations can lead to either
homogenization or differentiation, depending
homogenization and differentiation of fish faunas
Evidence for Homogenization or
Differentiation
Changes in similarity patterns of fish faunas have
been examined at a variety of spatial scales across
the United States, Canada, Europe, and Australia (Table 1). Overall, homogenization is a more
common phenomenon than differentiation
(Figure 2). A high degree of homogenization
was reported among six zoogeographic provinces in California where the average similarity, as
measured by Jaccard’s index, increased by 20.3%
(Marchetti et al. 2001). Similarly, the average
similarity among fish faunas in 10 major drainage basins in Iberia increased by 17.1% (Clavero
and García-Berthou 2006) and between two
river basins in Kansas by 15.4% (Eberle 2007).
An example of a high degree of differentiation
involves watersheds within the south coast zoogeographic province in California where the average similarity, as measured by Jaccard’s index,
decreased by 25.7% (Marchetti et al. 2001). It
should be noted that while the average change
in similarity among pairs of fish faunas in a region may indicate homogenization, some of the
pairwise comparisons may show differentiation.
For example, in Australia, the average change in
similarity among the 12 primary drainages was
3.0%, indicating overall homogenization (Olden et al. 2008). However, 14 of the 66 pairwise
combinations had a small negative change in
similarity, indicating slight differentiation in fish
faunas between some drainages.
80
Current similarity (%)
upon the spatial interplay of these two processes (Rahel 2002). Problems in assessing
changes in assemblage can arise when species
identity is not considered (i.e., increased species richness is used as a surrogate measure of
homogenization) or contemporary patterns of
community similarity are determined without
reference to historical patterns (Olden and
Rooney 2006).
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homogenization
70
15b
1
60
12
50
13a
6
40
4a
13b
4b
9
30
2
8a
8b
15a
20
14
10
differentiation
0
0
10
20
30
40
50
60
70
80
Past similarity (%)
Figure 2. A plot of past versus current average
similarities of fish faunas for various regions of
the world. The numbers refer to the study identification numbers in Table 1. Points above the diagonal indicate that fish faunas are more similar
today than in the past, thus homogenization has
occurred. Points below the diagonal indicate fish
faunas are less similar today than in the past, thus
differentiation has occurred. All the studies used
Jaccard’s index to quantify assemblage similarity
except for studies 12 (an unnamed similarity index) and 15 (Sorensen’s index).
Although changes in the percent similarity
among fish faunas provide a way to quantify
homogenization, the significance of a given
change in similarity can be reinforced if additional data are presented. For example, Rahel
(2000) noted that the average change in fish
faunas among the 48 contiguous states in the
United States was 7.2%. This change means
that, on average, any pair of states now shares
15.4 more fish species in common than they
did historically. Additionally, the 89 pairs of
states that had zero similarity (no species in
common), now have an average similarity of
12.2% and an average of 25 species in common. Among 10 river basins in Iberia, the
mean Jaccard similarity increased by 17% from
the pristine situation largely due to species
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introductions (Clavero and García-Berthou
2006). The magnitude of this change is apparent when you consider that, on average, more
than half (52.5%) of the species in each basin
are now nonnative.
Empirical Patterns and Mechanisms
Driving Homogenization and
Differentiation
Spatial Scale Dependence of
Homogenization versus Differentiation
Whether faunas have become more or less
similar over time may depend on the spatial
scale of the analysis. In several studies, homogenization was evident across larger spatial scales, whereas differentiation occurred
at intermediate spatial scales. For example,
homogenization was evident among the six
faunal provinces spanning California where
the average similarity increased from 15.7%
to 36.0% (Marchetti et al. 2001). By contrast,
within some of the provinces, differentiation
among watersheds occurred. An example is
the south coast province where average similarity among the 55 watersheds declined from
63.3% to 37.6% (compare 4a and 4b in Figure
2). In Canada, similarity increased at the provincial scale, but within the province of British Columbia, similarity decreased among the
eight ecoregions (compare 8a and 8b in Figure
2; Taylor 2004). In Australia, the similarity of
fish faunas increased among 12 major drainage
divisions spanning the continent but decreased
among the 53 watersheds within the northeast
coast drainage division (compare 15a and 15b
in Figure 2; Olden et al. 2008).
The most common explanation for the differentiation of faunas at intermediate spatial
scales is the idiosyncratic nature of species introductions. At larger spatial scales, it is likely that
a given nonnative species will be introduced
somewhere within each major basin, even if
it involves only one or a few sites. This means
that the introduced species will be counted as
present in most major basins and contribute
to an increase in similarity at that large spatial
scale. Within each major basin, the species may
be present in only a subset of watersheds, thus
contributing to differentiation at intermediate
spatial scales when the similarity among watersheds is analyzed. However, this differentiation
may be a transitory phenomenon as fish eventually spread through natural and human-assisted
means (Rahel 2004; Unmack, and Fagan 2004;
Johnson et al. 2008). For example, a strong
positive relationship between time since introduction and the number of occupied basins was
reported for nonnative fishes in the Iberian Peninsula (Clavero and García-Berthou 2006).
At small spatial scales, homogenization is
considered a more likely occurrence than differentiation (Marchetti et al. 2006). For example,
stream sites within a single watershed are likely
to share many of the same introduced species
when movement barriers are absent and habitat
degradation favors a few generalist species at the
expense of habitat specialists. Thus, homogenization of fish faunas has been reported for sites
in the Seine River basin in France (Boët et al.
1999), along the Biobio River in Chile (Habit
et al. 2006) and in the Etowah River basin in
Georgia, USA. (Walters et al. 2003). Despite
these generalities, the relationship between
spatial scale and changes in similarity can be
complex and dependent on historical biogeography (which influences the initial similarity of
faunas), the vagility of the species (which influences their ability to spread), and the cultural
history of a region (which determines which
species were introduced) (Cassey et al. 2007).
Role of Introductions versus
Extirpations
In theory, homogenization and differentiation
can be caused by introductions, extirpations, or
homogenization and differentiation of fish faunas
Translocated Species Cause
Homogenization; Exotic Species
Cause Differentiation
In studies of biotic homogenization, a distinction is often made between translocated species (i.e., species that are native somewhere in
the region but that have been moved to new
locations), and exotic species (i.e., species
not native to the region under study). For example, of the 901 fish introductions within the
48 coterminous United States reported by Rahel (2000), 673 involved translocated species
∆ similarity
48 states of United States
8
6
4
2
0
-2
7.3%
7.2%
-0.3%
Kansas vs. Arkansas river basins in Kansas
∆ similarity
a combination of both processes (Rahel 2002;
Olden and Poff 2003). In practice, changes in
faunal similarity seem to be mainly driven by
introductions that are much more common
than extirpations across a wide range of spatial
scales and geographic regions (Table 1). One
way to assess the relative importance of introductions versus extirpations is to determine
the change in similarity among faunas that
would occur due to each process acting separately. For example, if only introductions had
occurred among the 48 contiguous states of
the United States, the average change in similarity would be 7.3% (Figure 3). The change
due to extirpations alone would be –0.3%. The
effect of the two processes combined is 7.2%,
indicating that introductions are the major factor altering state fish faunas.
One place where extirpations appear to
play an important role in altering fish faunas
is in streams of the Great Plains of the United
States. These streams are naturally prone to
intermittency and extreme abiotic conditions
(Eberle 2007). These stresses have been exacerbated by water withdrawals and land use activities with the result that many native species
have been extirpated. In Kansas, introductions
or extirpations caused similar levels of homogenization, but their combined effects were synergistic (Figure 3).
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14.8%
15
10
7.1%
9.5%
5
0
Introductions
Extirpations
Both
Figure 3. Change in similarity due to introductions only, extirpations only, or both processes
combined. Top panel: Average change in similarity among 1,128 pairwise combinations of the 48
continuous United States involving 901 introduction events and 196 extirpation events (data from
Rahel 2000). Bottom panel: Change in similarity between the Kansas River and Arkansas River
drainages within the state of Kansas involving
26 introduction events and 13 extirpation events
(data from Eberle 2007).
such as largemouth bass, which are native to
eastern North America, whereas 228 involved
exotic species such as brown trout Salmo trutta,
which are native to Europe.
Some authors have reported that exotic
species tend to cause differentiation while
translocations tend to cause homogenization
among faunas (McKinney 2004; Leprieur et
al. 2008). The reason is that exotic species are
often introduced into a small number of sites,
making those sites unique compared to the
majority of sites. However, the differentiating
effect of exotic species is reduced as the species
spread and become shared among more sites.
In fact, an exotic species will tend to decrease
pairwise similarity among a set of sites until
half of the sites are occupied, after which the
continued spread of the species will increase
pairwise similarity, at least at the level of species
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∆ similarity (%)
occurrence data (Rooney et al. 2007). To the
extent that translocated species already occur at
many of the sites, their introduction to new sites
is likely to reduce the distinctness among sites,
thus contributing to homogenization.
Leprieur et al. (2008) noted that among
25 river basins across Europe, there was a general trend for introductions of exotic species to
cause differentiation, but for translocations of
species to cause homogenization (Figure 4).
This was because most translocated fish species
in Europe are native to eastern basins and were
widely introduced into less speciose drainages
of southern and Western Europe, thus contributing a large cosmopolitan element to the
overall fish faunas of European basins. By contrast, exotic species tended to be introduced
only into subsets of basins, thus enhancing the
regional distinctiveness of fish faunas. Such
exotic species include black bullhead Ameiurus melas and pumpkinseed Lepomis gibbosus,
which have been introduced mainly in Western
Europe; Amur sleeper Percottus glenii and black
carp Mylopharyngodon piceus, which have been
introduced mainly in eastern Europe; and western mosquitofish Gambusia affinis and eastern
mosquitofish G. holbrooki, which have been
6
25 river basins across Europe
5.0%
4
2.2%
2
0
-2
-1.6%
Translocations
Exotics
Both
Figure 4. Change in similarity between historic
and current fish faunas for 25 river basins across
Europe. Shown is the average change in similarity
that would have occurred if only species translocations had occurred, if only exotic species introductions had occurred, and the combined effect of
both processes. (Data from Leprieur et al. 2008).
introduced mainly in southern Europe. McKinney (2005) also reported that translocated
species caused homogenization while exotic
species tended to cause differentiation among
the fish faunas of 12 randomly selected states
in the United States.
Biotic Homogenization Caused by
Habitat Homogenization and
Degradation
The degradation and homogenization of habitats is thought to be a major cause of biotic
homogenization (McKinney 2006). Environmental homogenization can increase the speed
of species invasions and thus accelerate the
homogenization process (García-Ramos and
Rodríguez 2002). In aquatic systems, dams homogenize stream flow regimes by reducing variation in the timing, magnitude, duration, and
frequency of flooding and desiccation (Poff et
al. 2007). A constancy of flow regime can favor
widespread nonnative species at the expense of
endemic native species (Marchetti and Moyle
2001). Another common form of habitat homogenization is replacement of diverse stream
habitats (pools, riffles, runs, and side channels)
with the standing water habitat of reservoirs.
Often, native rheophyllic species are replaced
by a few widespread sport fishes that thrive in
the standing water habitat of reservoirs (Marchetti et al. 2001; Taylor et al. 2001). This was
clearly demonstrated in a comparison of fish assemblages among streams and reservoirs in the
Great Plains of the United States (Gido et al.
2009). The average similarity based on Jaccard’s
index among stream sites was 24.6%, whereas
the average similarity among reservoirs was
44.9% (Gido et al. 2009). Despite being located
in the same drainages as the stream sites, reservoir fish faunas were more homogeneous because they were dominated by a suite of lenticadapted species introduced for sport fishing. By
contrast, the stream sites retained a diverse suite
homogenization and differentiation of fish faunas
of rheophyllic species that varied geographically
due to historic, biogeographic factors. A situation where reservoir development contributed
to biotic differentiation was reported among
44 watersheds in California (Marchetti et al.
2006). In this case, the introduction of fishes to
reservoirs was idiosyncratic, with the result that
reservoirs were not dominated by the same set
of nonnative fishes. However, Marchetti et al.
noted that this result was scale-dependent, as
homogenization was noted at local scales (i.e.,
within a single drainage) and at very large scales
(i.e., between zoogeographic provinces).
Habitat degradation is another factor contributing to biotic homogenization. The percent
of a watershed in urban land use; the number of
canals, dams, or reservoirs; and the sediment
load in streams are often correlated with the
amount of biotic homogenization (Marchetti et
al. 2001; Walters et al. 2003; Olden et al. 2008).
In the southeastern United States, high amounts
of sediment favor a few cosmopolitan, tolerant
fish species at the expense of endemic species
that require clean gravels for foraging and reproduction (Walters et al. 2003; Scott 2006). In urban streams, a flashier hydrograph, elevated concentrations of nutrients and contaminants, and
altered channel morphology eliminate most fish
species except for a few tolerant forms (Boët et
al. 1999; Walsh et al. 2005). Often, habitat degradation facilitates invasions by a suite of nonnative species, further contributing to biotic
homogenization. Across North America, dominant species in urban waters include exotic species such as common carp and goldfish, as well
as translocated species such as green sunfish Lepomis cyanellus and bullheads.
Why Should We Care about Changes
in Biotic Similarity?
Homogenization or differentiation can be harbingers of conservation failures. Changes in bi-
319
otic similarity are caused by a combination of
species introductions and extirpations, both of
which are facilitated by habitat alterations. The
negative consequences of introductions and
habitat alterations on native biodiversity are
well known (Chapin et al. 2000). In many cases, homogenization is caused by introductions
of nonnative species rather than extirpations of
native species. Because of time lags in extirpations, introduced species can initially increase
local species richness without causing immediate loss of native species (Sax et al. 2002). Ultimately, however, the negative effects become
manifest, with the eventual decline or loss of
some native species (Ruesink 2003). For example, hybridization with introduced species
can lead to the eventual loss of endemic species but may occur over many years (Rhymer
and Simberloff 1996).
Biotic differentiation is often the result of
exotic species being introduced idiosyncratically in a few locations (Marchetti et al. 2001;
Leprieur et al. 2008). But differentiation is
likely to be a short-term phenomenon as nonnative species spread and increase the geographic extent over which negative effects are
likely to occur (Marchetti et al. 2006). Such an
expansion was documented in the Iberian Peninsula where the number of basins occupied by
various nonnative fish species was positively
correlated with elapsed time since the initial
introduction (Clavero and García-Berthou
2006). And secondary spread of nonnative
species accounted for 34% of the unauthorized
fish introductions reported in Wyoming (Rahel 2004). Fish communities in arid basins of
the southwestern United States have shown an
exponential increase in the number of reaches
with nonnative fishes and are predicted to converge toward dominance by nonnative species,
albeit with a time-lag reflecting differences in
the time course of introductions (Unmack and
Fagan 2004). Thus, given enough time, both
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homogenization and differentiation may converge on the same result, a few winners replacing many losers and the impoverishment of
global biodiversity (McKinney and Lockwood
1999; Scott 2006).
In addition to the loss of species diversity, taxonomic homogenization can have
other negative ecological and evolutionary
consequences. There is evidence that specialist species are more likely to be negatively affected by habitat degradation than generalist
species (Scott 2006; Devictor et al. 2008). The
replacement of ecological specialists by widespread generalists results in the functional homogenization of communities. Functional homogenization is of concern because it can alter
important ecosystem processes and reduce the
ability of communities to adapt to novel environmental conditions such as those associated with climate change (Chapin et al. 2000;
Olden et al. 2004). Furthermore, the loss of
spatial uniqueness reduces the raw material of
evolution by reducing spatial diversity in species composition and genetic make-up (Olden
et al. 2004; Williamson and May 2005).
Biotic homogenization often goes hand
in hand with cultural homogenization. Olden
et al. (2005) suggested that the increasingly
global uniformity in the Earth’s biota may be
linked to a loss of traditional values and have
important consequences for conservationoriented advocacy and ecotourism. In essence,
biological diversity, especially its endemic features, contributes to our sense of place and our
attachment to a particular geographic area.
This attachment is a critical component of our
psychological well-being and forms an important basis for conservation advocacy. Indeed,
the need to “save our wildlife heritage” is a
common theme in pleas for public support of
conservation actions. There are concerns that
biotic homogenization could reduce our sense
of place and thus weaken an important basis
for support of conservation efforts. Ecotourism might also suffer economic repercussions
from biotic homogenization. There will be less
incentive for tourists to travel great distances
to view biotas that are becoming increasingly
similar across the Earth.
Can We Slow or Reverse the
Homogenization Process?
Reducing the rate by which spatial patterns in
biodiversity are being altered will require controlling the three driving factors: introductions,
extinctions, and habitat homogenization. Historically, many introductions of nonnative fish
species were done by management agencies
to promote sportfishing. Agency-sponsored
introductions have declined in recent years
as natural resource managers have gained an
awareness of the problems nonnative species
can cause (Rahel 2004). Unfortunately, illegal
introductions remain a problem and public
education about the harmful effects of introduced species is needed. In some cases, it may
be possible to eliminate populations of nonnative species to facilitate the reestablishment of
native species (Lintermans 2000; Vredenburg
2004). Elimination of nonnatives may not be
possible in large rivers or lakes, but controlling the abundance of such species can help in
recovery efforts for native species (Tyus and
Saunders 2000).
Preventing species extinctions is crucial to
minimizing changes in spatial patterns of biodiversity. Unfortunately, widespread declines in
the distributions of native fishes are still occurring. An assessment of the conservation status
of North America’s fishes concluded that 39%
of the continent’s species are imperiled and
61 taxa (including subspecies) have become
extinct ( Jelks et al. 2008). Despite extensive
recovery efforts for endangered fishes, success
has been limited. Of 364 taxa listed as being of
homogenization and differentiation of fish faunas
conservation concern in 1989, only 8 had recovered enough to be removed from the list by
2008 ( Jelks et al. 2008). Efforts at preventing
the loss of native taxa will have to be increased
if further homogenization of the Earth’s biota
is to be slowed.
The third approach for reducing biotic homogenization is to minimize habitat alteration
and homogenization. Habitat preservation and
rehabilitation has long been a cornerstone for
recovery efforts of imperiled species. Habitat
alteration not only affects imperiled species directly through habitat loss, but also indirectly
by facilitating establishment of nonnative species (Marchetti et al. 2004). Consequently,
there is much interest in habitat restoration
efforts that help native species while simultaneously controlling nonnative species. Habitat improvements at the outflow of a desert
spring in the Mojave Desert converted a marsh
to flowing water habitat and changed the fish
composition from predominantly nonnative
sailfin molly Poecilia latipinna and western
mosquitofish to predominantly native Amargosa pupfish Cyprinodon nevadensis (Scoppettone et al. 2005). The natural-flow paradigm has been proposed as a landscape-level
approach for restoring native assemblages in
streams and rivers (Poff et al. 2007). The idea
is that restoring natural flow regimes will favor
native species that are better adapted to these
conditions than introduced species (Marchetti
and Moyle 2001; Moyle and Mount 2007).
Removing dams and their associated reservoirs is another approach for restoring native
biodiversity. Dam removal can facilitate recovery of native riverine species, many of which
are regionally endemic, while reducing the
abundance of nonnative species that are widespread in impoundments across North America (Kanehl et al. 1997; Johnson et al. 2008).
There is a need to develop quantitative models
that link land use change and water develop-
321
ment activities to environmental changes that,
in turn, predict the homogenization process.
Examples of such models include relating the
degree of homogenization to the proportion
of a watershed that has undergone anthropogenic modification (Marchetti et al. 2006) or
to changes in flow regimes, land use, or human infrastructures (Olden et al. 2008).
Reversing biotic homogenization will involve reversing species extirpations, species introductions, and habitat homogenization. One
way to restore historic patterns in biodiversity
is to restore habitat conditions to a more pristine state. Restoration of water quality in urban
streams can restore native fish assemblages.
Because urban streams are often dominated
by a few cosmopolitan and pollution-tolerant
fish species, habitat improvements that allow
recovery of regionally endemic species will
reverse the homogenization process. Consider
the case of the Scioto River in Columbus, Ohio
and the Cuyahoga River in Cleveland, Ohio
(Table 2). Prior to habitat improvements, both
rivers suffered from the urban river syndrome
(Walsh et al. 2005) and had fish assemblages
dominated by a few, pollution-tolerant taxa
(Table 2). Following improvements in water
quality and habitat conditions, additional species reappeared and the fish faunas became
less similar. Assemblage similarity based on
relative abundance data declined from 61% to
14%. Thus, habitat rehabilitation led to a reversal of the homogenization process.
Introduced predators can have dramatic
effects on fish biodiversity by eliminating or
reducing the abundance of numerous prey
species. For example, nonnative smallmouth
bass Micropterus dolomieu were found to homogenize fish assemblages in small North
American lakes by eliminating or reducing the
abundance of small-bodied prey species (MacRae and Jackson 2001). Experimentally reducing the population of smallmouth bass in an
322
rahel
Table 2. A comparison of fish assemblages in the Scioto River and Cuyahoga River before and after
habitat and water quality improvements. Shown are the total number of species collected by electrofishing and the proportional abundance of all species that constituted ≥1% of the total number of individuals captured. The similarity of the assemblages was calculated as percent similarity = ∑ minimum
(pi1, pi2) where pi1 is the proportion of the ith species in site 1 and pi2 is the proportion of the ith species
in site 2. The Scioto River was sampled at river mile 126.4 in 1979 and 2005. The Cuyahoga River was
sampled at river mile 15.9 in 1984 and 2000. Data provided by Dennis Mishne and Steven Tuckerman
of the Ohio Environmental Protection Agency.
Pre-recovery fish assemblages (percent similarity = 61%)
Scioto River (11 species)
Gizzard shad Dorosoma cepedianum
47%
Sunfishes Lepomis spp.
19%
Common carp Cyprinus carpio
17%
River carpsucker Carpiodes carpio
6%
Northern hog sucker Hypentelium nigricans 5%
Smallmouth buffalo Ictiobus bubalus 2%
Cuyahoga River (8 species)
Gizzard shad Sunfishes
Common carp
White sucker Catostomus commersonii
Creek chub Semotilus atromaculatus
Brown bullhead Ameiurus nebulosus
Freshwater drum Aplodinotus grunniens
51%
19%
13%
15%
2%
2%
2%
Post-recovery fish assemblages (percent similarity = 14%)
Scioto River (40 species)
Emerald shiner Notropis atherinoides
Sunfishes
River carpsucker
Gizzard shad
Smallmouth buffalo
Gravel chub Hybopsis x-punctata
Northern hog sucker Spotted bass Micropterus punctulatus
Common carp
Smallmouth bass
Spotfin shiner
Channel catfish Ictalurus punctatus Central stoneroller Sauger Sander canadensis
Cuyahoga River (25 species)
47%
Spotfin shiner Notropis spilopterus
19%
17%
Northern hog sucker
17%
7%
Bluntnose minnow Pimephales notatus
12%
4%
Central stoneroller Campostoma anomalum 8%
3%
Common shiner Luxilus cornutus
8%
3%
Smallmouth bass Micropterus dolomieu
7%
2%
White sucker
6%
2%
Common carp
6%
2%
Sand shiner Notropis stramineus
5%
1%
Sunfish
2%
1%
Gizzard shad
2%
1%
Greenside darter Etheostoma blennioides
1%
1%
1%
Adirondack lake allowed populations of native
littoral species to recover, indicating that homogenization could be reversed (Weidel et al.
2007). Removing nonnative fishes by netting
or electrofishing is time-consuming and expensive and must be repeated often to be effective (Weidel et al. 2007; Peterson et al. 2008).
In some situations, however, it may be possible
to use human fishers to achieve on-going control of nonnative predators. For example, in
Lake Victoria, intensive exploitation of Nile
perch Lates niloticus, a nonnative piscivore, has
allowed a resurgence by many native species
that were in decline or even thought to have
gone extinct (Balirwa et al. 2003). In a similar
vein, sustained exploitation of nonnative flathead catfish Pylodictis olivaris by recreational
or commercial fishers in a North Carolina river
may allow recovery of native fishes whose biomass was suppressed by up to 50% through
predation and competition (Pine et al. 2007).
The continual suppression of apex predators
needed to maintain native biodiversity may be
done more effectively through angler exploitation rather than through mechanical removal
by agency biologists.
homogenization and differentiation of fish faunas
Future Changes in Spatial Patterns of
Biodiversity
Homogenization of fish assemblages seems
likely to continue. Even the differentiation of
fish assemblages that has been observed at intermediate spatial scales seems to be a short-term
phenomenon that will be replaced by homogenization as nonnative species continue to spread
across the landscape. New patterns of global
commerce may allow biotic exchanges between
areas that had little opportunity for exchange in
the past. The construction of reservoirs, which
are hotspots for invasive species, seems likely
to continue ( Johnson et al. 2008). Continuing
declines in populations of native species seems
a likely scenario as the human footprint continues to grow across the Earth.
Perhaps the best hope for slowing or even
reversing the homogenization process lies in
habitat restoration. Recreating historical flow
regimes, improving water quality in urban rivers, or removing obsolete dams to recover flowing water habitats are ways to control nonnative
species while simultaneously restoring native
species. Continued education of the public
about the dangers of introducing nonnative species may help slow the homogenization process,
as will increasing the restrictions on the use of
live bait (Rahel 2004). We owe it to future generations to continue to work towards preserving
a sense of place for our aquatic environments.
Acknowledgments
Julian Olden and an anonymous reviewer provided helpful comments. Michael Marchetti
provided access to original data.
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